Abstract
Different distributions of ridged and smooth morphologies of Nucella emarginata
are found at wave-exposed and protected sites at China Point in Monterey Bay. A greater
number of the ridged morphology was found at the protected site and the smooth at the
exposed. Variation in drag coefficients, adhesive force, and crushing force between shell
morphologies do not appear to dictate this difference in distribution, although adhesive
force is marginally greater in wave exposed whelks. Predation on tethered whelks is
greater in the ridged morphology in general than the smooth. However, whelks were
eaten more quickly at the protected site, suggesting that wave action's effect on predators
may play a role in the distribution of the two morphologies. In a laboratory experiment,
crabs showed no preference between ridged or smooth N. emarginata, with a slight
preference for exposed whelks. Äfter 27 days of growth, it was unclear whether
differences in shell morphology were present among juveniles hatched from the exposed
site.
Introduction
An important issue in ecology is understanding how different genetic and
environmental factors dictate differences in the morphology of individuals within a
species. In turn it is important to see whether or not different morphologies lead to
greater or decreased individual fitness. Natural selection may act on genetically based
morphological variation to produce evolutionary change. Environmentally induced
phenotypic changes may have important effects at the population level.
Shell morphology is used as a rather broad term in the literature referring to
everything from architecture of the actual shell to differences in aperture width and
length. Morphological differences in the shell are often described as shell sculpture.
Differences in shell sculpture have been shown to protect against certain predators in
marine snails (e.g. Vermeij 1993). Differences in shell sculpture in bivalves has been
show to reduce drag in burrowing (e.g. Vermeij 1993). Clearly, morphological (and
specific sculptural) differences have the potential to affect fitness.
Nucella emarginata is a common predatory whelk found in rocky intertidal areas,
along the California coast. This species has direct development, juvenile snails hatch
from egg capsules attached to rock surfaces in the intertidal zone. Shell sculpture in N.
emarginata has been found to be under genetic control (e.g, Palmer 1984). However,
differences in shell morphology, specifically aperture thickness, have been found within
populations of N. emarginata, aperture thickness being a defense against crab predation
(Geller 1990). Whereas morphology can be genetic, crab presence has also been shown
to produce morphological changes in intertidal snails (e.g. Trussell 1996). Thus, while
shell sculpture can be a genetic trait, the possibility of predator induced phenotypic
plasticity remains to be answered for N. emarginata.
At China Point in Monterey Bay, California, two shell morphologies of Nucella
emarginata exist. A ridged morphology has raised axial ridges on the shell, while a
smooth morphology lacks these ridges and has a smooth outer shell. Preliminary
observations suggested that these two morphologies were unevenly distributed between
wave exposed and wave protected sites at China Point. More ridged snails were observed
in wave protected sites, and more smooth snails were observed in wave exposed sites.
In this study, I examined several factors that could be influencing the different
distributions of N. emarginata morphologies. Wave impact could be dictating these
different distributions by ripping off one morphology with greater drag. Wave impact
could also be affecting the predators of the snails. The main predators of N. emarginata
at China point are the crab Cancer antennarius and the Pisaster ochraceus, particularly
at the wave exposed site. Power supplied by breaking waves has been shown to protect
intertidal residents by knocking away their enemies or preventing them from feeding
(Leigh et al. 1987). Crab predation at the exposed site could be similarly affected because
in more wave exposed sites crab have a harder time locomoting and therefore feeding.
Differences in the crushing forces tolerated by ridged and smooth snails could be
dictating a preference in crab predation and therefore affecting the distributions seen at
each site. Initial distributions at hatching must also be determined before we can
accurately gauge the affect of either wave impact or predation.
In this study the most significant factor found to affect the difference in
distribution was wave impact on predators. Whether distributions were the same at
hatching as at later in life was indeterminate in the time allotted for the study.
Methods & Materials
Morphology
Two distinct shell morphologies of Nucella emarginata were examined: smooth
and ridged. Ridged morphologies have raised axial ridges of varying degrees. Smooth
morphologies have smooth shells lacking any such ridges. While some intermediate
morphologies were found, I focused my study on N. emarginata with distinct
morphologies. N. emarginata's shell morphology was compared in sites with differing
wave impact. A wave-exposed site was selected in Monterey Bay at the western edge of
China Point, and a protected site at Fisher beach, near the Monterey Bay Aquarium. I
quantified the difference in shell morphology at these sites by choosing at each site a 2 m
by 1 m rock area with a great concentration of N. emarginata, and counting the number
of each shell morphology present in that area.
Drag
To assess the potential impact of waves, the drag coefficient was measured for
each morphology. To this end, I collected five ridged-morphology N. emarginata from
the protected site and five smooth from the exposed site. These whelks were boiled and
their soft bodies removed. Each snail was then glued with five-minute epoxy to the
plastic plate of a drag transducer and placed in a high-speed wind tunnel. The plate of the
transducer was held flush with the wall of the tunnel to simulate the orientation of the
snail in surf-zone flow. The drag imposed by wind was transduced to a voltage and
recorded using a voltmeter. The direction of greatest drag was determined, and force
readings were taken at five different wind speeds: 21.4 m/s, 28.9 m/s, 36.4 m/s, 43.9 m/s
and 51.3 m/s. Profile area for each snail was determined by taking a digital picture of the
snail next to an object of a known surface area. The object and the snail were cut out of
the paper print-out and weighed. Profile area was determined using the ratio of paper
weight to area. With this information in hand, the drag coefficient could be determined
for each shell.
Drag Coefficient =
(2 *Drag Force)
(Air density* Profile Area* (Velocity/2))
A two-tailed t test at a wind speed of 36.4 was used to determine whether a significant
difference existed between the average drag coefficients of the two morphologies.
Adhesive Force
The adhesive force of N. emarginata was compared between the exposed and the
protected sites by pulling off approximately 40 whelks at each site. Whelks were pulled
off in the direction of greatest drag. Two different force meters were used to record
adhesive force, one with a 500 g rating for whelks below 14 mm long, the other with a 5
kg rating for bigger whelks. A string was attached to the force meter with a loop and the
other end was secured with a noose around the whelk's shell. The meter was then used to
tug on the snail, and the dislodgment force was recorded. For whelks that were too small,
or oriented in a position making it difficult to use the noose technique, the string was
glued to the whelk's shell using cyanoacrylate adhesive. N. emarginata that were
accessible and feeding on acorn barnacles were selected for these tests because whelks
tend to hold on with greatest force while feeding.
Crushing Force
The force to crush shells (a simulation of predation by crabs) was measured on
twenty whelks, ten from each site and five of each morphology. Crushing was
standardized to larger crab predation, which involves crushing of the shell with one claw,
as opposed to smaller crabs that peel away at the aperture lip of the snail (Bertness and
Cunningham 1981). One jaw of a pair of pliers was held steady by a vise and the snail
was placed between this stationary jaw and the movable jaw. A 5 kg force meter was
then used to forcibly close the pliers until the aperture was crushed, and the crushing
force was recorded. Each whelk was grasped in the same orientation and the meter was
placed at approximately the same spot to avoid complications due to a variable lever arm.
Tethering
To examine predation at each site, twenty whelks, ten of each morphology, were
transplanted from protected to exposed sites and vice versa. Fishing snap swivels were
glued with epoxy to the whelk's shells and were attached with fishing line to bolts in the
lower intertidal zone, just below the whelk's normal vertical distribution. Two snails of
each morphology were tethered to each bolt at approximately the same level in the
intertidal zone. Snails were checked 1,3 and 6 days after tethering.
Crab Predation and Influence
To analyze predation in the lab as well as to test for an effect of crab presence on
shell growth, three crabs (Cancer antennarius approx. carapace width 5-8 cm) were
collected and placed in Tupperware*“ containers (25*25 cm) with mesh cutouts to allow
water flow. These Tupperware"M containers were then weighted with rocks and placed
into a larger dish tub with water flowing in. Three control tubs were also set up in
random order along the line of water flow. Eight whelks of similar length were placed in
each of the crab and no-crab containers, four whelks from each site (two of each
morphology), marked for their site of origin. Influence of crab effluent on whelks was
determined in smaller 1-liter containers (Figure 1). Water was siphoned into these
containers with plastic tubing from the larger tubs containing either a crab or no crab.
Two containers with whelks from protected and exposed sites were set up for each larger
tub. Four whelks of similar size (shell lengths - approx. 16 mm- 18 mm) were placed in
each smaller container and individually labeled with nail polish. Initial and final readings
were taken of length and width of the aperture at approximately the same position on the
shell. Two notches were filed into the outer lip of the body whorl of each whelk to
determine whether growth had occurred. Whelks were fed bay mussels (Mytilus
trossulus) of approximately the same (shell length = approx. 20 mm to 22 mm).
Hatching
To test for differences in initial shell morphology distribution, I collected six sets
of egg cases from four different egg clusters from both the exposed and the protected site
and kept them in tea strainers. Only the egg cases from the exposed site hatched so 20
whelks from each of the four exposed containers were transferred to four new tea
strainers and placed in containers with flowing seawater. The baby whelks were fed the
smallest available mussel recruits (M. trossulus); mussels were increased in size as the
snails grew. Snails maintained in this fashion were held for 27 days, at which time their
morphology was assessed.
Results
Morphology
There was a larger fraction of ridged shells at the protected site than at the
exposed site (Figure 2).
Drag
The drag coefficients for smooth and ridged snails were not statistically different
(two-tailed test, t=7.9, p» 0.05). At a wind speed of 36.4 m/s (equivalent to a water
velocity of 3.2 m/s), the average drag coefficient for smooth snails was 0.630 with a
standard error of 0.009. The average drag for ridged was 0.648 with a standard error of
0.019.
Adhesive Force
The difference in adhesive force between ridged and smooth snails was not
significantly different. Statistical significance was determined by conducting an
ANCOVA with site as the variant and whelk shell length as a covariant. Although there
was no difference between morphologies (ANCOVA, F= 0.218, p =.642), a significant
difference in adhesive force was found between snails at the two sites (ANCOVA, F =
7.698, p = 0.007) (Figure 3). The protected snails averaged 3.30 N while the exposed
snails averaged 4.71 N.
Crushing Force
No significant difference in crushing force was found between the two
morphologies, or between the two sites (ANCOVA, F = 1.013, p = 0.330). Average
crushing force for exposed snails was 23.72 N (Standard Error, SE-4.43). Average
crushing force for protected snails was 21.22 N (SE- 2.01). For ridged shells, the
average crushing force was 22.94 N (SE-3.54), and average crushing force for smooth
shells was 22.23 N (SE-3.60).
Tethering
A greater number of ridged snails were eaten at both the protected and the
exposed sites, as seen in Figure 4. Over the 6 days of the experiment wave intensity
varied, with larger waves on days 1-3 and low wave intensity on days 4-6. Exposed
whelks were eaten at a greater rate during calmer wave activity, while protected snails
were eaten at a relatively steady rate. Two predators, crabs and Pisaster, fed on exposed
snails, while the protected snails had evidence only of crab predation. Fragments of shell
attached to line suggested crab predation, whereas empty shells attached to line suggested
Pisaster.
Crab Predation
In the laboratory experiment, crabs showed no preference for either ridged or
smooth snails. Crabs chose to eat exposed snails first 4 out of 6 times (p = 0.23), but
showed no further consistent preference for exposed or protected snails. No increase in
the thickness of the aperture lip was seen in either crab-exposed snails or control snails.
A significant difference (ANOVA, F=15.14, p-0.008) was seen in drilling rates between
control snails and those under crab influence with crab f3 excluded (Table 1). This crab
was unable to feed on whelks because it had lost half a claw. Whelks exposed to water
flow from a tank of actively feeding crabs ate the least amount of mussels; twelve of
these whelks didn’t feed at all (Figure 5).
Hatching
In the 27 days of this experiment, the hatched N. emarginata had not grown
enough to distinguish between ridged or smooth morphologies. The whelks grew from 1
mm at time of hatching to 3 mm after 27 days. They also developed banding of
coloration, and some initial signs of ridges or architecture, however if was impossible to
discern different morphologies because all appeared the same.
Discussion
Wave impact on different shell morphologies of Nucella emarginata does not
seem to dictate their ability to live in wave exposed or wave protected conditions. The
drag coefficient is not significantly different, so the drag on the two different
morphologies of the same size snail is approximately the same. Therefore, the greater
abundance of smooth snails at the wave exposed site cannot be explained by lessened
drag on the smooth morphology. The adhesive force between the two morphologies does
not differ as would be expected if this force were a selective factor. However, the
average adhesive force of the wave exposed N. emarginata gives them a greater ability to
adhere in conditions of greater wave impact. This difference could be related to
differences in foot size (Trussell 1997).
Although wave impact on the snail itself cannot explain the different distributions
of morphologies, its effect on predation appears to be a viable explanation. The crushing
force of shells did not vary between the two sites, nor did it vary between morphologies.
Therefore, the ability of the crab to crush shells is unlikely to dictate a preference by this
predator. In the laboratory the crabs did not significantly favor snails of a particular
morphology or those from a particular site, suggesting that crabs at China Point would
not eat more of one type of N. emarginata. However, the tethering experiment yielded
different results.
The tethering experiment was conducted over a period of 6 days, the first three of
which were wavy, and the last three of which were extremely calm. During the first three
days, only one snail was eaten at the exposed site while eight were eaten at the protected
site. These wavy days may have made it difficult for crab predators to prey upon the
tethered snails at the exposed site. In contrast, on the calm days 8 more snails were eaten
at the exposed site, while feeding rates stayed approximately the same at the protected
site. The calm conditions may have allowed crab predators greater access to snail prey at
the exposed site. Bigger waves and greater wave impacts at the exposed site limit crab
mobility in the intertidal zone (Leigh et al. 1987). This suggests that the intensity of crab
predation may be dictated by wave conditions.
The contradictory results to the above experiments lay in the preference for ridged
snails at the exposed site; many more ridged snails than smooth snails were eaten. At the
exposed site eight out of the nine snails eaten were ridged. This could be due to
unforeseen differences between predation in a laboratory experiment as opposed to
predation in the field. Ridged snails may be easier for crabs to grasp than smooth snails.
This could explain the greater abundance of smooth snails at the exposed site. However,
a preference for ridged snails was also observed at the protected site, leaving
uncertainties as to the factors dictating distributions of different morphologies there.
While it is therefore probable that crab predation plays a key role in the different
distribution of ridged and smooth N. emarginata, this factor cannot explain all
distribution results.
Plastic response to crab presence was indeterminate in these experiments due to
the lack of feeding by many of the snails under crab influence. No similar trend was seen
in the control snails, suggesting that crab presence causes decreased feeding rate in snails.
The snails in the presence of the crab with half a claw had similar feeding rates to control
snails, suggesting that crabs must be actively feeding on snails to have an affect. This
experiment would have to be run for a longer period to see if snails add thicker shell in
response to crabs despite lack of feeding. Crab effluent has been shown to cause snails to
grow thicker shells in Littorina obtusa (Trussell 1996).
The next step is to determine, by hatching and raising N. emarginata, if the
underlying assumption of equal distribution for each population holds. If distributions at
hatching are determined, crab predation could be shown to play a significant role.
Results in the field suggest that there may be an advantage to having a smooth shell. It
this is under genetic control, natural selection may favor smooth shells, and they could
become more prevalent unless there are other advantages to having a ridged shell.
Conclusion
The direct impact of environment on the snail is not a major factor in the
distribution of their shell morphology. In contrast, while different distributions of ridged
and smooth Nucella emarginata were not explained completely, wave impact on
predators of these snails seems to be very plausible explanation. To further explain why
different morphologies of N. emarginata were seen in different numbers at these two
sites, initial distributions would have to be determined. That information could clarify
some of the inconsistencies in this experiment as well as the literature as to whether shell
sculpture is exclusively genetic, or also a plastic trait.
Acknowledgments
This project owes a lot to the help of my advisors Mark Denny, Eric Sanford and Jim
Watanabe. I would like to thank Mark Denny for always listening to and answering my
numerous questions, as well as his creative ideas for how I was actually going to test all
my hypotheses. Thanks to Eric Sanford for all his time and help with my experimental
set-ups and ideas, from catching crabs to interpreting results. Thanks to Jim Watanabe
for all his statistics help, as well as thoughtful suggestions along the way. I would also
like to thank Carrie Kappel for always volunteering her time. I would also like to thank
my Dad for helping me collect over 200 snails on his vacation.
Literature Cited
Bertness, M.D. and C. Cunningham. 1981. Crab shell crushing predation and gastropod
architectural defenses. Journal of Experimental Marine Biology and Ecology
Vol. 50 no. 2-3: 213-230.
Geller, Jonathon B. 1990. Consequences of a morphological defense: growth, repair and
reproduction by thin and thick-shelled morphs of Nucella emarginata. Journal of
Experimental Marine Biology and Ecology. Vol.144, no.2,3: 173-184.
Leigh Jr., Egbert G, Robert T. Paine, James F. Quinn and Thomas H. Suchanek. 1987.
Wave energy and intertidal productivity. National Academy of Sciences
Proceedings Vol. 84, no. 5: 1314-1318.
Palmer, Richard A. 1984. Species Cohesiveness and genetic control of shell color and
form in Thais emarginata. Malacologia Vol 25, no 2: 477-491.
Trussell, Geoffrey C. 1996. Phenotypic plasticity in an intertidal snail: The role of the
common crab predator. Evolution Vol 50, no 1: 448-454.
Trussell, Geoffrey. 1997. Phenotypic plasticity in the foot size of an intertidal snail.
Ecology Vol 78, no. 4: 1033-1048.
Vermeij, Geerat J. 1993. A Natural History of Shells. New Jersey: Princeton University
Press.
Table 1:Analysis of Variance for differences in drilling rate
between whelks of different sites and either under the
influence of crabs or controls.
Dep Var:Drilling n:10
Multiple R: 0.87
Source
Sum of Squares
Mean-Square F-ratio
15.14
Treat
98.82
98.82
Whelks
0.42
0.06
0.42
Treat Whelks
20.42
20.42
0.008
0.81
0.13
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure Legends
Experimental set- up for crab predation and crab influence on snails.
Predator preference for snail morphologies was assessed in the large
containers, whereas effects of crabs on whelks was quantified in smaller
containers with water flowing from the tubs. See text for details.
Distribution of ridged and smooth morphologies of Nucella emarginata in
samples taken at the wave exposed (n-62) and wave protected (n-62)
areas. Black represents the ridged morphology while striped represents
the smooth.
The difference in the average adhesion between snails from the wave
exposed and the wave protected areas. Exposed whelks had a greater
adhesion force on average.
Predation on tethered Nucella after-1, 3 and 6 days attached in the low
intertidal zone. Days 1-3 had wavy conditions and days 4-6 were calm.
Black represents snails transplanted from the wave exposed area to the
waye protected area while striped represents snails transplanted from the
waye protected area to the wave exposed area.
Differences in drilling rates between snails under crab influence and
control snails. Black represents snails from the wave exposed site and
stripes represent snails from the wave protected site. Crab-exposed snails
fed significantly less than control snails.
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